Identification of neural progenitor cells and their progeny reveals long distance migration in the developing octopus brain

Abstract

Cephalopods have evolved nervous systems that parallel the complexity of mammalian brains in terms of neuronal numbers and richness in behavioral output. How the cephalopod brain develops has only been described at the morphological level, and it remains unclear where the progenitor cells are located and what molecular factors drive neurogenesis. Using histological techniques, we located dividing cells, neural progenitors and postmitotic neurons in Octopus vulgaris embryos. Our results indicate that an important pool of progenitors, expressing the conserved bHLH transcription factors achaete-scute or neurogenin, is located outside the central brain cords in the lateral lips adjacent to the eyes, suggesting that newly formed neurons migrate into the cords. Lineage-tracing experiments then showed that progenitors, depending on their location in the lateral lips, generate neurons for the different lobes, similar to the squid Doryteuthis pealeii. The finding that octopus newborn neurons migrate over long distances is reminiscent of vertebrate neurogenesis and suggests it might be a fundamental strategy for large brain development.

Cephalopod Retinal Development Shows Vertebrate-like Mechanisms of Neurogenesis

“…However, no pseudostratification of the lateral lips has been described. Cephalopod central nervous system development may more closely resemble neurogenesis found in other invertebrates or molluscs (Deryckere et al, 2021;Marthy, 1987).…”

“…Although pseudostratified neurogenesis is found in the cephalopod retina, there is little evidence that the cell biology of chordal or central nervous system neurogenesis is similar. It has been reported that cells migrate from the lateral lip in the cephalopod embryo to regions within the brain (Deryckere et al, 2021). However, no pseudostratification of the lateral lips has been described.…”

“…This includes a lack of expression of the canonical neurogenic ELAV, DpElav-1, in the retina, an RNA binding protein commonly found in differentiating neurons across species (Akamatsu et al, 2005;Denes et al, 2007; N. P. Meyer & Seaver, 2009;Nakanishi et al, 2012;Nomaksteinsky et al, 2009). bHLH factors NeuroD and NeuroG, which both have roles in neural specification and differentiation in many animals and are expressed in the lateral lips and brain in D. pealeii and other cephalopods, are completely absent for the retina (Supplemental Figure 1) (Buresi et al, 2013;Deryckere et al, 2021;Shigeno et al, 2015). However, it has been reported in Octopus vulgaris that achaetescute homolog Ov-ascl1, a third proneural bHLH transcription factor, is expressed in the retina (Deryckere et al, 2021).…”

“…Although pseudostratified neurogenesis is found in the cephalopod retina, the cell biology of chordal or central nervous system neurogenesis is still not well described. It has been reported that cells migrate from the lateral lip tissue, an embryonic neurogenic tissue found in the cephalopod embryo to regions within the brain but pseudostratification of the lateral lips is not apparent (Deryckere et al, 2021). Cephalopod central nervous system development may more closely resemble neurogenesis found in other invertebrates or molluscs (Deryckere et al, 2021;Marthy, 1987).…”

“…It has been reported that cells migrate from the lateral lip tissue, an embryonic neurogenic tissue found in the cephalopod embryo to regions within the brain but pseudostratification of the lateral lips is not apparent (Deryckere et al, 2021). Cephalopod central nervous system development may more closely resemble neurogenesis found in other invertebrates or molluscs (Deryckere et al, 2021;Marthy, 1987). With a central nervous system composed of significantly more cells than other Spiralians and requiring long distance cell migration, it is likely that cephalopods have evolved lineage specific mechanisms to manage this process.…”